Skip to main content
SpringerLink
Log in

Isolation, characterization and PCR multiplexing of microsatellite loci for two sub-species of terrestrial isopod Porcellio dilatatus (Crustacea, Oniscidea)

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Several microsatellite markers have already been developed for different terrestrial isopod species such as Armadillidium vulgare, A. nasatum and Porcellionides pruinosus. In all these species, the endosymbiont Wolbachia has a feminizing effect that generates a female bias in sex ratio and reduces the number of reproductive males. Thus this can potentially decrease the genetic diversity of host populations. However, in some other isopod species, Wolbachia induces cytoplasmic incompatibility (CI); the most commonly described effect of Wolbachia in arthropods. The CI by rendering some crossings incompatible can reduce the gene flow and strengthen genetic differentiation between isopod populations. To date, the influence of Wolbachia inducing CI on population structure of terrestrial isopods has never been investigated. In this study, we developed 10 polymorphic microsatellite markers shared by two sub-species of Porcellio dilatatus. Crossings between the two sub-species are partially incompatible due to two CI-inducing Wolbachia strains. These new microsatellite markers will allow us to investigate the effect of CI on host genetic differentiation in this species complex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  • Barbara T, Palma-Silva C, Paggi GM, Bered F, Fay MF, Lexer C (2007) Cross-species transfer of nuclear microsatellite markers: potential and limitations. Mol Ecol 16:3759–3767

    Article  PubMed  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France)

  • Bouchon D, Cordaux R, Grève P (2008) Feminizing Wolbachia and the evolution of the sex determination in isopods. In: Bourtzis K, Miller T (eds) Insect symbiosis, vol 3. CRC Press, Boca Raton, pp 273–294

    Chapter  Google Scholar 

  • Cordaux R, Bouchon D, Grève P (2011) The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends Genet 27:332–341

    Article  CAS  PubMed  Google Scholar 

  • Cordaux R et al (2012) Widespread Wolbachia infection in terrestrial isopods and other crustaceans. Zookeys 176:123–131

    Article  PubMed  Google Scholar 

  • Dittmer J, Beltran-Bech S, Lesobre J, Raimond M, Johnson M, Bouchon D (2014) Host tissues as microhabitats for Wolbachia and quantitative insights into the bacterial community in terrestrial isopods. Mol Ecol 23:2619–2635

    Article  CAS  PubMed  Google Scholar 

  • Durand S, Beauché F, Richard F, Beltran-Bech S (2015) How do females’ genetic characteristics influence male mate preference in the terrestrial isopod Armadillidium vulgare? Ethology 121:1122–1130

    Article  Google Scholar 

  • Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327

    Article  PubMed  Google Scholar 

  • Giraud I, Valette V, Bech N, Grandjean F, Cordaux R (2013) Isolation and characterization of microsatellite loci for the isopod crustacean Armadillidium vulgare and transferability in terrestrial isopods. PLoS One 8:e76639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www2.unil.ch/popgen/softwares/fstat.htm

  • Grandjean F, Gouin N, Verne S, Delaunay C, Patri S (2005) Characterization of polymorphic microsatellite loci in the terrestrial isopod Porcellionides pruinosus. Mol Ecol Notes 5:507–509

    Article  CAS  Google Scholar 

  • Grant PR (1998) Evolution on islands. Oxford University Press, Oxford

    Google Scholar 

  • Jaenike J, Dyer KA, Cornish C, Minhas MS (2006) Asymmetrical reinforcement and Wolbachia infection in Drosophila. PLoS Biol 4:e325

    Article  PubMed  PubMed Central  Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci India B 86:6196–6200

    Article  CAS  Google Scholar 

  • Legrand J, Juchault P, Artault J, Mocquard J, Picaud J (1974) Le statut systématique de la « forme » petiti Vandel de Porcellio dilatatus Brandt, récoltée à l’île Saint-Honorat (Alpes-Maritimes). Critères morphologiques, génétiques et physiologiques. Bull Soc Zool Fr 99:461–471

    Google Scholar 

  • Legrand J, Martin G, Artault J (1978) Correlation between the presence of a bacterial symbiont in oocytes of Porcellio dilatatus petiti, and the sterility of the cross: P.d. petiti male x P.d. dilatatus female. Arch Inst Pasteur Tunis 55:507–514

    CAS  PubMed  Google Scholar 

  • Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457:830–836

    Article  CAS  PubMed  Google Scholar 

  • Malausa T et al (2011) High-throughput microsatellite isolation 238 through 454 GS-FLX Titanium pyrosequencing of enriched DNA libraries. Mol Ecol Resour 11:638–644

    Article  CAS  PubMed  Google Scholar 

  • Masson S et al (2014) Development of a microsatellite primer set to investigate the genetic population structure of Armadillidium nasatum (Crustacea, Oniscidea). J Genet 93:545–549

    Article  PubMed  Google Scholar 

  • Meglecz E, Costedoat C, Dubut V, André G, Malausa T, Pech N, Martin JF (2010) QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics 26:403–404

    Article  CAS  PubMed  Google Scholar 

  • Michel-Salzat A, Bouchon D (2000) Phylogenetic analysis of mitochondrial LSU rRNA in oniscids. CR Acad Sci III Vie 323:827–837

    Article  CAS  Google Scholar 

  • Michel-Salzat A, Cordaux R, Bouchon D (2001) Wolbachia diversity in the Porcellionides pruinosus complex of species (Crustacea: Oniscidea): evidence for host-dependent patterns of infection. Heredity 87:428–434

    Article  CAS  PubMed  Google Scholar 

  • Moret Y, Juchault P, Rigaud T (2001) Wolbachia endosymbiont responsible for cytoplasmic incompatibility in a terrestrial crustacean: effects in natural and foreign hosts. Heredity 86:325–332

    Article  CAS  PubMed  Google Scholar 

  • Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol 4:535–538

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Sherman PW, Seeley TD, Reeve HK (1988) Parasites, pathogens, and polyandry in social hymenoptera. Am Nat 131:602–610

    Article  Google Scholar 

  • Sicard M et al (2014) Bidirectional cytoplasmic incompatibility caused by Wolbachia in the terrestrial isopod Porcellio dilatatus. J Invertebr Pathol 121:28–36

    Article  PubMed  Google Scholar 

  • Telschow A, Hammerstein P, Werren JH, Gavrilets S (2005) The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation. Evolution 59:1607–1619

    Article  PubMed  Google Scholar 

  • Telschow A, Flor M, Kobayashi Y, Hammerstein P, Werren JH (2007) Wolbachia-induced unidirectional cytoplasmic incompatibility and speciation: mainland-island model. PLoS One 2:e701

    Article  PubMed  PubMed Central  Google Scholar 

  • Verne S, Puillandre N, Brunet G, Gouin N, Samollow PB, Anderson JD, Grandjean F (2006) Characterization of polymorphic microsatellite loci in the terrestrial isopod Armadillidium vulgare. Mol Ecol Notes 6:328–330

    Article  CAS  Google Scholar 

  • Verne S, Moreau J, Caubet Y, Bouchon D, Johnson M, Grandjean F (2007) Male mating success during parturial intermoults in the terrestrial isopod Armadillidium vulgare revealed by the use of a microsatellite locus. J Crustacean Biol 27:217–219

    Article  Google Scholar 

  • Verne S, Johnson M, Bouchon D, Grandjean F (2012) Effects of parasitic sex-ratio distorters on host genetic structure in the Armadillidium vulgare-Wolbachia association. J Evol Biol 25:264–276

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to thank Daniel Guyonnet for technical assistance, Tiffany Laverre and Victorien Valette for providing samples of Po. pruinosus, Po. cingindus, P. scaber, P. dispar and C. convexus and Mine Altinli for checking the English in the paper. This work was supported by the french Ministère de l’Enseignement Supérieur et de la Recherche and the CNRS.

Author information

Author notes

    Authors and Affiliations

    1. Laboratoire EBI Ecologie & Biologie des Interactions - UMR CNRS 7267, Equipe Ecologie, Evolution, Symbiose, Université de Poitiers, Bât. B8-B35, 5 rue Albert Turpin, TSA 51106, 86022, Poitiers Cedex 9, France

      Caroline Michaud, Cassandre Chupeau, Nicolas Bech, Magali Thierry, Pierre Greve & Sophie Beltran-Bech

    2. Institut des Sciences de l’Evolution de Montpellier (UMR CNRS-IRD-UM 5554), Université de Montpellier, Place Eugène Bataillon, 34095, Montpellier, France

      Mathieu Sicard

    Authors
    1. Caroline Michaud
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Cassandre Chupeau
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Nicolas Bech
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Magali Thierry
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Mathieu Sicard
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Pierre Greve
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Sophie Beltran-Bech
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Sophie Beltran-Bech.

    Ethics declarations

    Conflict of interest

    The authors declare that they have no conflict of interest.

    Additional information

    Caroline Michaud and Cassandre Chupeau have contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (PDF 104 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Michaud, C., Chupeau, C., Bech, N. et al. Isolation, characterization and PCR multiplexing of microsatellite loci for two sub-species of terrestrial isopod Porcellio dilatatus (Crustacea, Oniscidea). Genetica 144, 223–228 (2016). https://doi.org/10.1007/s10709-016-9892-3

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10709-016-9892-3

    Keywords

    Search

    Navigation